The ‘peptidome’ of tumour-derived chaperone-rich cell lysate anti-cancer vaccines reveals potential tumour antigens that stimulate tumour immunity

References

• Sharma P, Wagner K, Wolchok JD, Allison JP. Novel cancer immunotherapy agents with survival benefit: Recent successes and next steps. Nat Rev Cancer 2011;11:805–12
   PubMed Web of Science ®Google Scholar
• Lesterhuis WJ, Haanen JB, Punt CJ. Cancer immunotherapy – Revisited. Nat Rev Drug Discov 2011;10:591–600
   PubMed Web of Science ®Google Scholar
• Hammerstrom AE, Cauley DH, Atkinson BJ, Sharma P. Cancer immunotherapy: Sipuleucel-T and beyond. Pharmacotherapy 2011;31:813–28
   PubMed Web of Science ®Google Scholar
• Wood C, Srivastava P, Bukowski R, Lacombe L, Gorelov AI, Gorelov S, et al. An adjuvant autologous therapeutic vaccine (HSPPC-96;vitespen) versus observation alone for patients at high risk of recurrence after nephrectomy for renal cell carcinoma: a multicentre, open-label, randomised phase III trial. Lancet 2008;372:145–54
   PubMed Web of Science ®Google Scholar
• Pilla L, Patuzzo R, Rivoltini L, Maio M, Pennacchioli E, Lamaj E, et al. A phase II trial of vaccination with autologous, tumor-derived heat-shock protein peptide complexes gp96, in combination with GM-CSF and interferon-alpha in metastatic melanoma patients. Cancer Immunol Immunother 2006;55:958–68
   PubMed Web of Science ®Google Scholar
• See AP, Pradilla G, Yang I, Han S, Parsa AT, Lim M. Heat shock protein-peptide complex in the treatment of glioblastoma. Expert Rev Vaccines 2011;10:721–31
   PubMed Web of Science ®Google Scholar
• Itoh K, Yamada A, Mine T, Noguchi M. Recent advances in cancer vaccines: An overview. Jpn J Clin Oncol 2009;39:73–80
   PubMed Web of Science ®Google Scholar
• Torigoe T, Tamura Y, Sato N. Heat shock proteins and immunity: Application of hyperthermia for immunomodulation. Int J Hyperthermia 2009;25:610–6
   PubMed Web of Science ®Google Scholar
• Feng H, Zeng Y, Graner MW, Katsanis E. Stressed apoptotic tumor cells stimulate dendritic cells and induce specific cytotoxic T cells. Blood 2002;100:4108–15
   PubMed Web of Science ®Google Scholar
• Feng H, Zeng Y, Graner MW, Likhacheva A, Katsanis E. Exogenous stress proteins enhance the immunogenicity of apoptotic tumor cells and stimulate antitumor immunity. Blood 2003;101:245–52
   PubMed Web of Science ®Google Scholar
• Murshid A, Gong J, Calderwood SK. Heat-shock proteins in cancer vaccines: Agents of antigen cross-presentation. Expert Rev Vaccines 2008;7:1019–30
   PubMed Web of Science ®Google Scholar
• Segal BH, Wang XY, Dennis CG, Youn R, Repasky EA, Manjili MH, et al. Heat shock proteins as vaccine adjuvants in infections and cancer. Drug Discov Today 2006;11:534–40
   PubMed Web of Science ®Google Scholar
• Srivastava P. Interaction of heat shock proteins with peptides and antigen presenting cells: chaperoning of the innate and adaptive immune responses. Annu Rev Immunol 2002;20:395–425
   PubMed Web of Science ®Google Scholar
• Zeng Y, Graner MW, Katsanis E. Chaperone-rich cell lysates, immune activation and tumor vaccination. Cancer Immunol Immunother 2006;55:329–38
   PubMed Web of Science ®Google Scholar
• Graner MW, Bigner DD. Chaperone proteins and brain tumors: Potential targets and possible therapeutics. Neuro-Oncology 2005;7:260–78
   PubMed Web of Science ®Google Scholar
• Demine R, Walden P. Testing the role of gp96 as peptide chaperone in antigen processing. J Biol Chem 2005;280:17573–78
   PubMed Web of Science ®Google Scholar
• Fleischer K, Schmidt B, Kastenmuller W, Busch DH, Drexler I, Sutter G, et al. Melanoma-reactive class I-restricted cytotoxic T cell clones are stimulated by dendritic cells loaded with synthetic peptides, but fail to respond to dendritic cells pulsed with melanoma-derived heat shock proteins in vitro. J Immunol 2004;172:162–9
   PubMed Web of Science ®Google Scholar
• Nicchitta CV. Re-evaluating the role of heat-shock protein-peptide interactions in tumour immunity. Nat Rev Immunol 2003;3:427–32
   PubMed Web of Science ®Google Scholar
• Gullo CA, Teoh G. Heat shock proteins: To present or not, that is the question. Immunol Lett 2004;94:1–10
   PubMed Web of Science ®Google Scholar
• Baker-LePain JC, Sarzotti M, Fields TA, Li CY, Nicchitta CV. GRP94 (gp96) and GRP94 N-terminal geldanamycin binding domain elicit tissue nonrestricted tumor suppression. J Exp Med 2002;196:1447–59
   PubMed Web of Science ®Google Scholar
• Reits E, Griekspoor A, Neijssen J, Groothuis T, Jalink K, van Veelen P, et al. Peptide diffusion, protection, and degradation in nuclear and cytoplasmic compartments before antigen presentation by MHC class I. Immunity 2003;18:97–108
   PubMed Web of Science ®Google Scholar
• European Medicines Agency. Withdrawal Assessment Report for Oncophage. London, 2009. Available from: http://www.emea.europa.eu/docs/en_GB/document_library/Application_withdrawal_assessment_report/2010/03/WC500075459.pdf
   Google Scholar
• Graner M, Raymond A, Akporiaye E, Katsanis E. Tumor-derived multiple chaperone enrichment by free-solution isoelectric focusing yields potent antitumor vaccines. Cancer Immunol Immunother 2000;49:476–84
   PubMed Web of Science ®Google Scholar
• Graner MW, Zeng Y, Feng H, Katsanis E. Tumor-derived chaperone-rich cell lysates are effective therapeutic vaccines against a variety of cancers. Cancer Immunol Immunother 2003;52:226–34
   PubMed Web of Science ®Google Scholar
• Zeng Y, Feng H, Graner MW, Katsanis E. Tumor-derived, chaperone-rich cell lysate activates dendritic cells and elicits potent antitumor immunity. Blood 2003;101:4485–91
   PubMed Web of Science ®Google Scholar
• Zeng Y, Graner MW, Katsanis E. Chaperone-rich cell lysates, immune activation and tumor vaccination. Cancer Immunol Immunother 2005
   PubMed Web of Science ®Google Scholar
• Li G, Andreansky S, Helguera G, Sepassi M, Janikashvili N, Cantrell J, et al. A chaperone protein-enriched tumor cell lysate vaccine generates protective humoral immunity in a mouse breast cancer model. Mol Cancer Ther 2008;7:721–9
   PubMed Web of Science ®Google Scholar
• Graner MW, Cumming RI, Bigner DD. The heat shock response and chaperones/heat shock proteins in brain tumors: Surface expression, release, and possible immune consequences. J Neurosci 2007;27:11214–27
   PubMed Web of Science ®Google Scholar
• Li G, Zeng Y, Chen X, Larmonier N, Sepassi M, Graner MW, et al. Human ovarian tumour-derived chaperone-rich cell lysate (CRCL) elicits T cell responses in vitro. Clin Exp Immunol 2007;148:136–45
   PubMed Web of Science ®Google Scholar
• Bleifuss E, Bendz H, Sirch B, Thompson S, Brandl A, Milani V, et al. Differential capacity of chaperone-rich lysates in cross-presenting human endogenous and exogenous melanoma differentiation antigens. Int J Hyperthermia 2008;24:623–37
   PubMed Web of Science ®Google Scholar
• Epple LM, Bemis LT, Cavanaugh RP, Skope A, Mayer-Sonnenfeld T, Frank C, et al. Prolonged remission of advanced bronchoalveolar adenocarcinoma in a dog treated with autologous, tumour-derived chaperone-rich cell lysate (CRCL) vaccine. Int J Hyperthermia, 2013;29:390-8
   Google Scholar
• Zeng Y, Graner MW, Thompson S, Marron M, Katsanis E. Induction of BCR-ABL-specific immunity following vaccination with chaperone-rich cell lysates derived from BCR-ABL+ tumor cells. Blood 2005;105:2016–22
   PubMed Web of Science ®Google Scholar
• Kislin KL, Marron MT, Li G, Graner MW, Katsanis E. Chaperone-rich cell lysate embedded with BCR-ABL peptide demonstrates enhanced anti-tumor activity against a murine BCR-ABL positive leukemia. Faseb J 2007
   PubMed Web of Science ®Google Scholar
• He L, Feng H, Raymond A, et al. Dendritic-cell-peptide immunization provides immunoprotection against BCR-ABL-positive leukemia in mice. Cancer Immunol Immunother 2001;50:31–40
   PubMed Web of Science ®Google Scholar
• Rotzschke O, Falk K, Wallny HJ, Faath S, Rammensee HG. Characterization of naturally occurring minor histocompatibility peptides including H-4 and H-Y. Science 1990;249:283–7
   PubMed Web of Science ®Google Scholar
• Falk K, Rotzschke O, Stevanovic S, Jung G, Rammensee HG. Allele-specific motifs revealed by sequencing of self-peptides eluted from MHC molecules. Nature 1991;351:290–6
   PubMed Web of Science ®Google Scholar
• Haynes PA, Fripp N, Aebersold R. Identification of gel-separated proteins by liquid chromatography-electrospray tandem mass spectrometry: Comparison of methods and their limitations. Electrophoresis 1998;19:939–45
   PubMed Web of Science ®Google Scholar
• Cui JW, Li WH, Wang J, Li AL, Li HY, Wang HX, et al. Proteomics-based identification of human acute leukemia antigens that induce humoral immune response. Mol Cell Proteomics 2005;4:1718–24
   PubMed Web of Science ®Google Scholar
• Raghavan M, Wijeyesakere SJ, Peters LR, Del Cid N. Calreticulin in the immune system: Ins and outs. Trends Immunol 2013;34:13–21
   PubMed Web of Science ®Google Scholar
• Junker N, Kvistborg P, Kollgaard T, Straten P, Andersen MH, Svane IM. Tumor associated antigen specific T-cell populations identified in ex vivo expanded TIL cultures. Cell Immunol 2012;273:1–9
   PubMed Web of Science ®Google Scholar
• Fellenberg F, Hartmann TB, Dummer R, Usener D, Schadendorf D, Eichmuller S. GBP-5 splicing variants: New guanylate-binding proteins with tumor-associated expression and antigenicity. J Invest Dermatol 2004;122:1510–17
   PubMed Web of Science ®Google Scholar
• Chumpitazi BF, Bouillet L, Drouet MT, Kuhn L, Garin J, Zarski JP, et al. Biological autoimmunity screening in hepatitis C patients by anti-HepG2 lysate and anti-heat shock protein 70.1 autoantibodies. Eur J Clin Microbiol Infect Dis 2009;28:137–46
   PubMed Web of Science ®Google Scholar
• Zappasodi R, Bongarzone I, Ghedini GC, Castagnoli L, Cabras AD, Messina A, et al. Serological identification of HSP105 as a novel non-Hodgkin lymphoma therapeutic target. Blood 2011;118:4421–30
   PubMed Web of Science ®Google Scholar
• Mojtahedi Z, Safaei A, Yousefi Z, Ghaderi A. Immunoproteomics of HER2-positive and HER2-negative breast cancer patients with positive lymph nodes. OMICS 2011;15:409–18
   PubMed Web of Science ®Google Scholar
• Paez MC, Matsuura E, Diaz LA, Shoenfeld Y, Serrano NC, Anaya JM. Laminin-1 (LM-111) in preeclampsia and systemic lupus erythematosus. Autoimmunity 2013;46:14–20
   PubMed Web of Science ®Google Scholar
• Scanlan MJ, Welt S, Gordon CM, Chen YT, Gure AO, Stockert E, et al. Cancer-related serological recognition of human colon cancer: identification of potential diagnostic and immunotherapeutic targets. Cancer Res 2002;62:4041–7
   PubMed Web of Science ®Google Scholar
• Gosney JR, Williams IJ, Dodson AR, Foster CS. Morphology and antigen expression profile of pulmonary neuroendocrine cells in reactive proliferations and diffuse idiopathic pulmonary neuroendocrine cell hyperplasia (DIPNECH). Histopathology 2011;59:751–62
   PubMed Web of Science ®Google Scholar
• Padua RA, Larghero J, Robin M, le Pogam C, Schlageter MH, Muszlak S, et al. PML-RARA-targeted DNA vaccine induces protective immunity in a mouse model of leukemia. Nat Med 2003;9:1413–7
   PubMed Web of Science ®Google Scholar
• Yokoe T, Tanaka F, Mimori K, Inoue H, Ohmachi T, Kusunoki M, et al. Efficient identification of a novel cancer/testis antigen for immunotherapy using three-step microarray analysis. Cancer Res 2008;68:1074–82
   PubMed Web of Science ®Google Scholar
• Barbaric D, Byth K, Dalla-Pozza L, Byrne JA. Expression of tumor protein D52-like genes in childhood leukemia at diagnosis: Clinical and sample considerations. Leuk Res 2006;30:1355–63
   PubMed Web of Science ®Google Scholar
• Pontes ER, Matos LC, da Silva EA, Xavier LS, Diaz BL, Small IA, et al. Auto-antibodies in prostate cancer: humoral immune response to antigenic determinants coded by the differentially expressed transcripts FLJ23438 and VAMP3. Prostate 2006;66:1463–73
   PubMed Web of Science ®Google Scholar
• Wojcik C, DeMartino GN. Intracellular localization of proteasomes. Int J Biochem Cell Biol 2003;35:579–89
   PubMed Web of Science ®Google Scholar
• Lin HH, Ray S, Tongchusak S, Reinherz EL, Brusic V. Evaluation of MHC class I peptide binding prediction servers: Applications for vaccine research. BMC Immunol 2008;9:8
   PubMed Web of Science ®Google Scholar
• Moroi Y, Mayhew M, Trcka J, Hoe MH, Takechi Y, Hartl FU, et al. Induction of cellular immunity by immunization with novel hybrid peptides complexed to heat shock protein 70. Proc Natl Acad Sci USA 2000;97:3485–90
   PubMed Web of Science ®Google Scholar
• Flechtner JB, Cohane KP, Mehta S, Slusarewicz P, Leonard AK, Barber BH, et al. High-affinity interactions between peptides and heat shock protein 70 augment CD8+ T lymphocyte immune responses. J Immunol 2006;177:1017–27
   PubMed Web of Science ®Google Scholar
• Blachere NE, Li Z, Chandawarkar RY, Suto R, Jaikaria NS, Basu S, et al. Heat shock protein-peptide complexes, reconstituted in vitro, elicit peptide-specific cytotoxic T lymphocyte response and tumor immunity. J Exp Med 1997;186:1315–22
   PubMed Web of Science ®Google Scholar
• Chang CX, Dai L, Tan ZW, Choo JA, Bertoletti A, Grotenbreg GM. Sources of diversity in T cell epitope discovery. Front Biosci 2011;16:3014–35
   Web of Science ®Google Scholar
• Vabulas RM, Ahmad-Nejad P, Ghose S, Kirschning CJ, Issels RD, Wagner H. Hsp70 as endogenous stimulus of the toll/interleukin-1 receptor signal pathway. J Biol Chem 2002;277:15107–12
   PubMed Web of Science ®Google Scholar
• Tamura Y, Torigoe T, Kukita K, Saito K, Okuya K, Kutomi G, et al. Heat-shock proteins as endogenous ligands building a bridge between innate and adaptive immunity. Immunotherapy 2012;4:841–52
   PubMed Web of Science ®Google Scholar
• Asea A, Kabingu E, Stevenson MA, Calderwood SK. HSP70 peptidembearing and peptide-negative preparations act as chaperokines. Cell Stress Chaperones 2000;5:425–31
   PubMed Web of Science ®Google Scholar
• Zeng Y, Chen X, Larmonier N, Li G, Sepassi M, Marron M, et al. Natural killer cells play a key role in the antitumor immunity generated by chaperone-rich cell lysate vaccination. Int J Cancer 2006;119:2624–31
   PubMed Web of Science ®Google Scholar
• Nieland TJ, Tan MC, Monne-van Muijen M, Koning F, Kruisbeek AM, van Bleek GM. Isolation of an immunodominant viral peptide that is endogenously bound to the stress protein gp96/GRP94. Proc Natl Acad Sci USA 1996;93:6135–9
   PubMed Web of Science ®Google Scholar
• Lammert E, Arnold D, Nijenhuis M, Momburg F, Hämmerling GJ, Brunner J, et al. The endoplasmic reticulum-resident stress protein gp96 binds peptides translocated by TAP. Eur J Immunol 1997;27:923–7
   PubMed Web of Science ®Google Scholar
• Arnold D, Faath S, Rammensee H, Schild H. Cross-priming of minor histocompatibility antigen-specific cytotoxic T cells upon immunization with the heat shock protein gp96. J Exp Med 1995;182:885–9
   PubMed Web of Science ®Google Scholar
• Suto R, Srivastava PK. A mechanism for the specific immunogenicity of heat shock protein-chaperoned peptides. Science 1995;269:1585–8
   PubMed Web of Science ®Google Scholar
• Meng SD, Gao T, Gao GF, Tien P. HBV-specific peptide associated with heat-shock protein gp96. Lancet 2001;357:528–9
   PubMed Web of Science ®Google Scholar
• Ishii T, Udono H, Yamano T, et al. Isolation of MHC class I-restricted tumor antigen peptide and its precursors associated with heat shock proteins Hsp70, Hsp90, and gp96. J Immunol 1999;162:1303–9
   PubMed Web of Science ®Google Scholar
• Stocki P, Wang XN, Morris NJ, Dickinson AM. Hsp70 natively and specifically associates with an N-terminal dermcidin-derived peptide that contains an HLA-A*03 antigenic epitope. J Biol Chem 2011;286:12803–11
   PubMed Web of Science ®Google Scholar
• Parker KC, Bednarek MA, Coligan JE. Scheme for ranking potential HLA-A2 binding peptides based on independent binding of individual peptide side-chains. J Immunol 1994;152:163–75
   PubMed Web of Science ®Google Scholar
• Rammensee H, Bachmann J, Emmerich NP, Bachor OA, Stevanovic S. SYFPEITHI: Database for MHC ligands and peptide motifs. Immunogenetics 1999;50:213–9
   PubMed Web of Science ®Google Scholar
• Buus S, Lauemoller SL, Worning P, Kesmir C, Frimurer T, Corbet S, et al. Sensitive quantitative predictions of peptide-MHC binding by a ‘Query by Committee’ artificial neural network approach. Tissue Antigens 2003;62:378–84
   PubMed Web of Science ®Google Scholar
• Nielsen M, Lundegaard C, Worning P, et al. Reliable prediction of T-cell epitopes using neural networks with novel sequence representations. Protein Sci 2003;12:1007–17
   PubMed Web of Science ®Google Scholar
• Reche PA, Reinherz EL. Prediction of peptide-MHC binding using profiles. Methods Mol Biol 2007;409:185–200
   PubMedGoogle Scholar
• Van Durme J, Maurer-Stroh S, Gallardo R, Wilkinson H, Rousseau F, Schymkowitz J. Accurate prediction of DnaK-peptide binding via homology modelling and experimental data. PLoS Comput Biol 2009;5:e1000475
   PubMed Web of Science ®Google Scholar
• Udono H, Ichiyanagi T, Mizukami S, Imai T. Heat shock proteins in antigen trafficking – Implications on antigen presentation to T cells. Int J Hyperthermia 2009;25:617–25
   PubMed Web of Science ®Google Scholar
• Binder RJ, Kelly JBIII, Vatner RE, Srivastava PK. Specific immunogenicity of heat shock protein gp96 derives from chaperoned antigenic peptides and not from contaminating proteins. J Immunol 2007;179:7254–61
   PubMed Web of Science ®Google Scholar
• Oura J, Tamura Y, Kamiguchi K, Kutomi G, Sahara H, Toshihiko T, et al. Extracellular heat shock protein 90 plays a role in translocating chaperoned antigen from endosome to proteasome for generating antigenic peptide to be cross-presented by dendritic cells. Int Immunol 2011;23:223–37
   PubMed Web of Science ®Google Scholar
• Wang XY, Sun X, Chen X, Facciponte J, Repasky E, Kane J, et al. Superior antitumor response induced by large stress protein chaperoned protein antigen compared with peptide antigen. J Immunol 2010;184:6309–19
   PubMed Web of Science ®Google Scholar
• Subjeck JR, Shyy T, Shen J, Johnson RJ. Association between the mammalian 110,000-Dalton heat-shock protein and nucleoli. J Cell Biol 1983;97:1389–95
   PubMed Web of Science ®Google Scholar
• Calvert ME, Digilio LC, Herr JC, Coonrod SA. Oolemmal proteomics – Identification of highly abundant heat shock proteins and molecular chaperones in the mature mouse egg and their localization on the plasma membrane. Reprod Biol Endocrinol 2003;1:27
   PubMedGoogle Scholar
• Easton DP, Kaneko Y, Subjeck JR. The Hsp110 and Grp1 70 stress proteins: Newly recognized relatives of the Hsp70s. Cell Stress Chaperones 2000;5:276–90
   PubMed Web of Science ®Google Scholar
• Cantrell J, Larmonier C, Janikashvili N, Bustamante S, Fraszczak J, Herrell A, et al. Signaling pathways induced by a tumor-derived vaccine in antigen presenting cells. Immunobiology 2010;215:535–44
   PubMed Web of Science ®Google Scholar
• Larmonier N, Cantrell J, Lacasse C, Li G, Janikashvili N, Situ E, et al. Chaperone-rich tumor cell lysate-mediated activation of antigen-presenting cells resists regulatory T cell suppression. J Leukoc Biol 2008;83:1049–59
   PubMed Web of Science ®Google Scholar